Utilizing sponge spicules in taxonomic, ecological and environmental reconstructions: a review Magdalena Łukowiak Department of Environmental Paleobiology, Institute of Paleobiology, Polish Academy of Sciences, Warsaw, Poland ABSTRACT Most sponges produce skeletons formed by spicules, structural elements that develop in a wide variety of sizes and tridimensional shapes. The morphologies of spicules are often unique to clade- or even species-level taxa which makes them particularly useful in taxonomic assignments. When dead sponge bodies disintegrate, spicules become incorporated into sediments and sometimes accumulate into enormous agglomerations called spicule mats or beds, or fossilize to form special type of rocks called the spiculites. The record of fossil and subfossil sponge spicules is extraordinarily rich and often serves as a basis for far-reaching reconstructions of sponge communities, though spicules are also bearers of significant ecological and environmental information. Specific requirements and preferences of sponges can be used to interpret the environment in which they lived, and reconstruct oscillations in water depths, pH, temperatures, and other parameters, providing snapshots of past climate conditions. In turn, the silicon isotope compositions in spicules (δ30Si) are being increasingly often used to estimate the level of silicic acid in the marine settings throughout the geological history, which enables to reconstruct the past silica cycle and ocean circulation. This contribution provides a review of the use of sponge spicules in reconstructions of sponge communities, their ecology, and environments, and aims to detect the pertinent gaps in their utilization. Even though spicules are well known for their significance as bearers of Submitted 2 July 2020 Accepted 27 November 2020 taxonomic, ecological, and environmental data, their potential remains to be fully Published 18 December 2020 exploited. Corresponding author Magdalena Łukowiak, Subjects Ecology, Marine Biology, Taxonomy, Zoology, Aquatic and Marine Chemistry [email protected] Keywords Porifera, Sponge spicules, Spicular analysis, Paleoenvironment, Marine and freshwater Academic editor chemistry, Silica fractionation, Silicon isotopes Blanca Figuerola Additional Information and INTRODUCTION Declarations can be found on page 19 Sponges (Porifera) are a species-rich clade of the earliest-diverging metazoans (Wörheide DOI 10.7717/peerj.10601 et al., 2012), with a global distribution (van Soest et al., 2012), diverse ecologies and functions (Wulff, 1984, 2006; Bell, 2008; Maldonado, Ribes & Van Duyl, 2012; De Goeij Copyright 2020 Łukowiak et al., 2013; Goeij, Lesser & Pawlik, 2017), and a record spanning at least the entire Distributed under Phanerozoic (Reitner & Wörheide, 2002). Among the four sub-clades of Porifera, Creative Commons CC-BY 4.0 three (Demospongiae, Hexactinellida, and Homoscleromorpha) produce skeletons of How to cite this article Łukowiak M. 2020. Utilizing sponge spicules in taxonomic, ecological and environmental reconstructions: a review. PeerJ 8:e10601 DOI 10.7717/peerj.10601 amorphous silica (Hooper & Van Soest, 2002) and one (Calcarea) of magnesium-calcite (Rossi et al., 2014). These skeletons are composed of elements called spicules (Uriz et al., 2003; Sethmann & Wörheide, 2008). Spicules provide structural support for maintaining the vertical body position, minimize the metabolic cost of water exchange (Riisgard & Larsen, 1995; Uriz et al., 2003), and may even deter predators (Uriz et al., 2003 and the literature cited therein). They often develop in different sizes (Hooper & Van Soest, 2002) and a wide variety of tridimensional shapes, with many being unique to clade- or even species-level taxa. Demosponges are characterized by spicules of monaxonic or tetraxonic symmetry (Hooper & Van Soest, 2002). Hexactinellids produce spicules of hexactinic or triaxonic (cubic) symmetry or shapes that are clearly derived from such morpohologies (Leys, Mackie & Reiswig, 2007). The spicules of homoscleromorphs represent peculiar tetractines (calthrops) and their derivatives that originate through reduction or ramification of the clads (Muricy & Díaz, 2002). Spicules of Calcarea are produced in three basic forms: diactines, triactines and tetractines (Manuel et al., 2002). The mineral composition of sponge spicules makes these structures the most resistant parts of the sponge bodies (Uriz, 2006) and ensures the ability of spicules to withstand various taphonomic processes (Rützler & Macintyre, 1978; Łukowiak, Pisera & O’Dea, 2013), resulting in that they often constitute the only evidence of the presence of some sponges in an ecosystem (Łukowiak, 2016b). Even though sponges are often known from rich assemblages of bodily-preserved specimens (Volkmer- Ribeiro & Reitner, 1991; Olszewska-Nejbert & Świerczewska-Gładysz, 2013; Łukowiak & Pisera, 2016), a significant part of their fossil and subfossil record is also represented by their spicules. Having that in mind, spicules can be of crucial importance for reconstructions of extinct or cryptic (hiding in cervices and caves) sponge communities; and, indeed, they have been investigated especially with respect to their taxonomic significance (Díaz & Rützler, 2001; Hooper & Van Soest, 2002). The morphologies of spicules and their arrangement, together with other important sponge features, such as the shape, consistency, and color, are essential when identifying sponges (Collin et al., 2005). In contrast to whole-bodied sponge fossils, spicules are common in many depositional environments (Pisera, 2006). Their significance, however, is often underestimated, which is mostly due to the difficulties in assigning disassociated spicules to sponge taxa or due to the scarcity of the material. Despite that numerous studies reviewed the current knowledge of various neontological (Manconi & Pronzato, 2015) and paleontological (Pisera, 1999) aspects of sponges, including their importance for evolutionary, ecological, and environmental reconstructions (Harrison, 1988b; Pisera, 2004, 2006; Sim-Smith, Ellwood & Kelly, 2017; De Freitas Oliveira, Da Costa & Benedito, 2020), spicules alone—though discussed to some degree in all these studies—were given considerably less attention (Cohen, 2003; Pronzato, Pisera & Manconi, 2017). For instance, Harrison (1988a) and Frost (2001) discussed the utilization of freshwater sponge spicules in paleolimnological studies. Łukowiak (2020), PeerJ, DOI 10.7717/peerj.10601 2/30 Table 1 The number of records obtained through Google Scholar and PubMed using the search terms “sponge spicules”, “glass ramp”, “spiculite” and “spongillite”. Term Sponge spicules Glass ramp Spiculite Spongillite Records Relevant Records Relevant Records Relevant Records Relevant Google Scholar 18,500 (184: in title) 28 150 12 1130 35 47 15 PubMed 367 6 58 0 1 0 0 0 Other than that, however, sponge spicules have never been the subject of a detailed review that would summarize their utility in paleontological and neontological studies. The purpose of the present contribution is to review the use of loose sponge spicules (that is, those disassociated with sponge bodies), a widespread component in fossil, subfossil, and recent marine and freshwater settings, in reconstructions of extinct and modern sponge communities, their ecologies, and environments. SURVEY METHODOLOGY So far there were no comprehensive reviews concerning the use of freshwater and marine sponge spicules. To provide an overview of the most relevant articles dealing with the application of sponge skeletal elements in taxonomic, ecological, and environmental studies I went through the records of Google Scholar and PubMed. I used the search terms “sponge spicules”, “glass ramp”, “spiculite”,and“spongillite” (see Table 1 for the numbers of obtained records). Note that the term “sponge spicules” returns a very high number of records in Google Scholar. The results were examined one- by-one and the vast majority of the records turned out to be irrelevant for the present paper. Therefore, additional search was conducted, this time limited only to works containing the searched term in the title. The online search was performed in August 2020. Expectedly, the records from both databases overlapped. Each record was further explored in detail and additional references were obtained from the literature cited in these works. The literature that was not available online—mostly printed-only manuscripts from the first half of the 20th century and old, 19th century classic paleontological works—were obtained through the Library of the Institute of Paleobiology, Polish Academy of Sciences, Warsaw, Poland. Following the survey, I compiled a database (Supplemental Information 1) comprising a list of the most relevant articles (including the year of publication, authorship, language of the publication, type of environment [marine/freshwater], type of studies (e.g., related to sponge taxonomy, water properties, climate etc.), geographic area of investigation, and the age of the investigated material). In the sections below, I discuss the papers that appear to be of special relevance for the present contribution. In these papers, the disassociated sponge spicules had to be (i) the only, (ii) the main, or (iii) a noteworthy component used for the taxonomic, ecological, and environmental studies. Despite that efforts weremadetoprovideanexhaustivelistofstudies,itcannotberulesoutthatsome relevant papers were unintentionally omitted, for example due to their absence